Alpine Botany

, Volume 129, Issue 2, pp 163–174 | Cite as

Wild cherry (Prunus avium (L.) L.) leaf shape and size variations in natural populations at different elevations

  • Danijela MiljkovićEmail author
  • Milena Stefanović
  • Saša Orlović
  • Milena Stanković Neđić
  • Lazar Kesić
  • Srđan Stojnić
Original Article


Leaf shape variations and developmental instability were examined for the first time in natural populations of Prunus avium (L.) L. in the central Balkan region (Bosnia and Herzegovina) at different elevational points, from 230 to 1177 m. above sea level. Geometric morphometric tools were applied to assess the variability of leaf shapes and sizes, while a fluctuating asymmetry leaf index was used as a measure of leaf developmental instability. According to the results of canonical variate analysis for the symmetric component of shape variation and hierarchical analysis of variance for centroid size, the studied populations could be partially differentiated into three groups. The co-variation between leaf form (shape and size) and climate variables was significant, estimated by two-block partial least square analysis. Climate variables (the sum of precipitation in May and the De Martonne aridity index) mostly influenced leaf shape and size. A population situated at the highest elevation had the highest value for fluctuating asymmetry leaf index, which was an indication of developmental instability. High natural variability and interpopulation differences were observed for all studied leaf traits (leaf shape, centroid size, fluctuating asymmetry leaf index, leaf area, leaf length and width, petiole length). For well-known traditional morphometric measures (leaf area, leaf length, leaf width, and petiole length) in accordance with previous studies, intrapopulation variability was greater than interpopulation variability. For centroid size and the fluctuating asymmetry leaf index (measures used in geometric morphometrics) variability was higher among populations than within them. This indicates that geometric morphometrics could give new insights into infra-specific variability.


Developmental instability Fluctuating asymmetry Geometric morphometrics Leaf morphology Prunus avium (L.) L. 



This paper was achieved as part of the project “Biosensing Technologies and Global System for Long-Term Research and Integrated Management of Ecosystems” (III-43002) and “Evolution in heterogeneous environments: mechanisms of adaptation, biodiversity conservation and biomonitoring” (OI-173025) financed by the Ministry of Education and Science of the Republic of Serbia. We thank the anonymous reviewers for their careful reading of our manuscript and their valuable comments and suggestions. The authors wish to thank the English language editor, native speaker and teacher of English Mrs Esther Grace Helajzen for proofreading and revised text correction,.

Author contributions

DM, SO and SS designed the research. MSN and LK collected and scanned the specimens. DM performed digitalization of specimens and analysis of fluctuating asymmetry. MS conducted analysis of leaf size and shape. DM and MS wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 30 kb)
35_2019_227_MOESM2_ESM.docx (660 kb)
Supplementary material 2 (DOCX 659 kb)
35_2019_227_MOESM3_ESM.docx (86 kb)
Supplementary material 3 (DOCX 85 kb)


  1. Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399. CrossRefGoogle Scholar
  2. Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98(3):604–613. CrossRefGoogle Scholar
  3. Ballian D, Bogunić F, Čabaravdić A, Pekeč S, Franjić J (2012) Population differentiation in the wild cherry (Prunus avium L.) in Bosnia and Herzegovina. Period Biol 114:43–54.
  4. Baltas EA (2008) Climatic conditions and availability of water resources in Greece. Int J Water Resour D 24(4):635–649. CrossRefGoogle Scholar
  5. Bresson CC, Vitasse Y, Kremer A, Delzon S (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol 31(11):1164–1174. CrossRefPubMedGoogle Scholar
  6. Chitwood DH, Headland LR, Ranjan A, Martinez CC, Braybrook SA, Koenig DP, Sinha NR (2012) Leaf asymmetry as a developmental constraint imposed by auxin-dependent phyllotactic patterning. Plant Cell 24(6):2318–2327. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chitwood DH, Rundell SM, Li DY, Woodford QL, Yu TT, Lopez JR, Greenblatt D, Kang J, Londo JP (2016) Climate and developmental plasticity: interannual variability in grapevine leaf morphology. Plant Physiol 170(3):1480–1491. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Pooter H (2003) Handbook of protocols for standardised and easy measurement of plant functional traits worldwide. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51(4):335–380. CrossRefGoogle Scholar
  9. Demesure B, Comps B, Petit RJ (1996) Chloroplast DNA phylogeography of the common 670 beech (Fagus sylvatica L.) in Europe. Evolution 50:2515–2520. CrossRefPubMedGoogle Scholar
  10. Ducci F, De Cuyper B, De Rogatis A, Dufour J, Santi F (2013) Wild Cherry Breeding (Prunus avium L.). In: Pâques LE (ed) Forest tree breeding in Europe, vol 25. Springer, Dordrecht, pp 463–511CrossRefGoogle Scholar
  11. Franiel I (2008) Fluctuating asymmetry of Betula pendula Roth leaves: an index of environment quality. Biodiv Res Conserv 9(10):1897–2810Google Scholar
  12. Freeman DC, Brown ML, Duda JJ, Graraham JH, Emlen JM, Krzysik AJ, Balbach H, Kovacic DA, Zak JC (2005) Leaf fluctuating asymmetry, soil disturbance and plant stress: a multiple year comparison using two herbs, Ipomoea pandurate and Cnidoscoluss timulosus. Ecol Indic 5:85–95. CrossRefGoogle Scholar
  13. Gömöry D, Paule L, Gömöryová E (2011) Effects of microsite variation on growth and adaptive traits in a beech provenance trial. J For Sci 57:192–199. CrossRefGoogle Scholar
  14. Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Bot 2014:1–17. CrossRefGoogle Scholar
  15. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. CrossRefGoogle Scholar
  16. Hijmans RJ, Guarino L, Mathur P (2012) Manual of DIVA-GIS version 7.5Google Scholar
  17. Hovenden MJ, Vander Schoor JK (2006) The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii. New Phytol 169:291–297. CrossRefPubMedGoogle Scholar
  18. Kiełtyk P (2017) Variation of vegetative and floral traits in the alpine plant Solidago minuta: evidence for local optimum along an elevational gradient. Alp Bot 128:47–57. CrossRefGoogle Scholar
  19. Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357. CrossRefPubMedGoogle Scholar
  20. Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934. CrossRefGoogle Scholar
  21. Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22(11):569–574. CrossRefPubMedGoogle Scholar
  22. Kozlov MV, Cornelissen T, Gavrikov DE, Kunavin MA, Lama AD, Milligan JR, Zverev V, Zvereva EL (2017) Reproducibility of fluctuating asymmetry measurements in plants: sources of variation and implications for study design. Ecol Indic 73:733–740. CrossRefGoogle Scholar
  23. Lindgren B, Laurila A (2005) Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria. J Evol Biol 18(4):820–828. CrossRefPubMedGoogle Scholar
  24. Liu Y, Li Y, Song J, Zhang R, Yan Y, Wang Y, Du FK (2018) Geometric morphometric analyses of leaf shapes in two sympatric Chinese oaks: Quercus dentata Thunberg and Quercus aliena Blume (Fagaceae). Ann For Sci 75(4):90CrossRefGoogle Scholar
  25. Mal TK, Uveges JL, Turk KW (2002) Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecol Indic 1(3):189–195. CrossRefGoogle Scholar
  26. Meier IC, Leuschner C (2008) Leaf size and leaf area index in Fagus sylvatica Forests: competing effects of precipitation, temperature and nitrogen availability. Ecosystems 11(5):655–669. CrossRefGoogle Scholar
  27. Miljković D (2012) Developmental stability of Iris pumila flower traits: a common garden experiment. Arch Biol Sci 64:123–133. CrossRefGoogle Scholar
  28. Miljković D, Selaković S, Vujić V, Stanisavljević N, Radović S, Cvetković D (2018) Patterns of herbivore damage, developmental stability, morphological and biochemical traits in female and male Mercurialis perennis in contrasting light habitats. Alp Bot 128:193–206. CrossRefGoogle Scholar
  29. Mratinić E, Fotirić Akšić M, Jovković R (2012) Analysis of wild sweet cherry (Prunus avium L.) germplasm diversity in South-East Serbia. Genetika 44:259–268. CrossRefGoogle Scholar
  30. Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38(7):535–552. CrossRefGoogle Scholar
  31. Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Springer Kluwer, Dordrecht, pp 335–364CrossRefGoogle Scholar
  32. Palmer AR, Strobeck C (2003) Fluctuating asymmetry analysis revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 279–319Google Scholar
  33. Pescador DS, de Bello F, Valladares F, Escudero A (2015) Plant trait variation along an altitudinal gradient in mediterranean high mountain grasslands: controlling the species turnover effect. PLoS One 10(3):p.e0118876. CrossRefGoogle Scholar
  34. Popović V, Kerkez I (2016) Population variability of wild cherry (Prunus avium L.) in Serbia according to the leaf morphology. Šumarski list 140:347–355. CrossRefGoogle Scholar
  35. Rakonjac V, Mratini E, Jovković R, Fotiri M (2014) Analysis of morphological variability in wild cherry (Prunus avium L.) genetic resources from central Serbia. J Agric Sci Technol 16:151–162Google Scholar
  36. Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ (2014) Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol 28:37–45. CrossRefGoogle Scholar
  37. Reinhardt D (2005) Regulation of phyllotaxis. Int J Dev Biol 49:539–546. CrossRefPubMedGoogle Scholar
  38. Rohlf J (2016a) tpsUtil v 1.70 (computer program). Stony Brook University, New YorkGoogle Scholar
  39. Rohlf J (2016b) tpsDig2 v 2.26 (computer program). Stony Brook University, New YorkGoogle Scholar
  40. Russell K (2003) EUFORGEN Technical Guidelines for genetic conservation and use for wild cherry (Prunus avium). Drawings: Prunus avium.. International Plant Genetic Resources Institute, RomeGoogle Scholar
  41. Santi F, Muranty H, Dufour J, Paques LE (1998) Genetic parameters and selection in a multisite wild cherry clonal test. Silvae Genet 47(2–3):61–67Google Scholar
  42. SAS Institute, Inc. (2011) The SAS System for Windows, release 9.3. SAS Institute, CaryGoogle Scholar
  43. Seguí J, Lázaro A, Traveset A, Salgado-Luarte C, Gianoli E (2017) Phenotypic and reproductive responses of an Andean violet to environmental variation across an elevational gradient. Alp Bot 128:59–69. CrossRefGoogle Scholar
  44. Sheets HD, Zelditch M, Swiderski D (2002) Morphometrics software: IMP-Integrated morphometrics package.
  45. Šilić  Č (2005) Atlas of Dendroflora (trees and shrubs) in Bosnia and Herzegovina. Franjevacka kuca Masna Luka, Matica hrvatska Citluk, Citluk  Google Scholar
  46. Sørensen JG, Norry FM, Scannapieco AC, Loeschcke V (2005) Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatiifrom the new world. J Evol Biol 18:829–837. CrossRefPubMedGoogle Scholar
  47. Souza GM, Viana JDOF, Oliveira RFD (2005) Asymmetrical leaves induced by water deficit show asymmetric photosynthesis in common bean. Braz J Plant Physiol 17(2):223–227. CrossRefGoogle Scholar
  48. Stefanović M, Nikolić B, Matić R, Popović Z, Vidaković V, Bojović S (2017) Exploration of sexual dimorphism of Taxus baccata L. needles in natural populations. Trees 31:1697–1710. CrossRefGoogle Scholar
  49. Teeling C, Maxted N, Ford-Lloyd BV (2012) The challenges of modelling species distribution: a case study of wild cherry (Prunus avium L.) in Europe. In: Maxted M, Dulloo E, Ford-Lloyd BV, Frese L, Iriondo JM, Pinheiro de Carvalho MAA (eds) Agrobiodiversity conservation: securing the diversity of crop wild relatives and landraces. CABI, London, pp 29–35CrossRefGoogle Scholar
  50. Telhado C, Fernando AO, Silveira G, Fernandes W, Cornelissen T (2017) Fluctuating asymmetry in leaves and flowers of sympatric species in a tropical montane environment. Plant Spec Biol 32:3–12. CrossRefGoogle Scholar
  51. Temel F (2018) Leaf size variation in natural wild cherry (Prunus avium) populations in Turkey. Int J Agric Biol. CrossRefGoogle Scholar
  52. Tucić B, Miljković D (2010) Fluctuating asymmetry of floral organ traits in natural populations of Iris pumilafrom contrasting light habitats. Plant Spec Biol. 25:173–184. CrossRefGoogle Scholar
  53. Viscosi V, Fortini P, Slice DE, Loy A, Blasi C (2009) Geometric morphometric analyses of leaf variation in four oak species of subgenus Quercus (Fagaceae). Plant Biosyst 143:575–587. CrossRefGoogle Scholar
  54. Welk E, De Rigo D, Caudullo G (2016) Prunus avium in Europe: distribution, habitat, usage and threats. In: Mubareka S, Jonsson R, Rinaldi F, Azevedo J, de Rigo D, Sikkema R (eds) European Atlas of forest tree species. Publication Office of the European Union, Luxembourg, pp 140–141Google Scholar
  55. Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S et al (2017) Global climatic drivers of leaf size. Science 357(6354):917–921. CrossRefPubMedGoogle Scholar

Copyright information

© Swiss Botanical Society 2019

Authors and Affiliations

  1. 1.Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”University of BelgradeBelgradeSerbia
  2. 2.Department of Ecology, Institute for Biological Research “Siniša Stanković”University of BelgradeBelgradeSerbia
  3. 3.Institute of Lowland Forestry and EnvironmentUniversity of Novi SadNovi SadSerbia
  4. 4.Department of Forestry, Faculty of AgricultureUniversity of East SarajevoVlasenicaBosnia and Herzegovina

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